Ms Biden is the first witness in the case to testify that she believed he was abusing drugs in the month he purchased the Colt Cobra .38 revolver.
She was once tipped to be a future US first lady, as the spouse of Beau Biden, an Iraq war veteran with his sights on Delaware’s governor’s mansion, and even the White House.
But sitting across the courtroom from Hunter on Thursday, she described how her life took a dramatically different turn during the pair’s on-off relationship after Beau’s death.
She told the court that they were both using crack cocaine for a period in 2018, revisiting some of the most publicly humiliating episodes of Biden family drama as her father-in-law seeks re-election.
‘I’m embarrassed and ashamed’
“Who introduced you to it?” Leo Wise, prosecuting, asked.
“Hunter did,” she replied. He looked down at the defence table as she spoke.
“It was a terrible experience that I went through, and I’m embarrassed and ashamed, and I regret that period of my life,” she said, appearing nervous and speaking in clipped sentences.
She told the court she stopped using drugs in August of that year, but that Hunter continued. Jurors took copious notes as she spoke.
Ms Biden described discovering drug paraphernalia and the Colt revolver in Hunter’s car on Oct 23, and disposing of it in a bin outside a supermarket near her home in Wilmington.
“I realise it was a stupid idea now, but I was just panicking,” she said. “I didn’t want him to hurt himself or my kids to find it and hurt themselves.”
Texts prosecutors showed to jurors revealed how the pair scrambled in the fallout of the incident.
Prosecutors played surveillance footage of Ms Biden disposing of the gun and ammunition mid-morning, then later returning and frantically searching for it. The gun was no longer there, and the police were called.
“[Hunter] was angry with me,” Ms Biden told the court.
In one text, Hunter, whose father was already contemplating a presidential run, told her: “The f—— FBI, Hallie. It’s hard to believe anyone is that stupid.”
“I’m sorry, I just want you safe. That was not safe,” she replied.
Under cross-examination, Abbe Lowell, defending, elicited an acknowledgement from Ms Biden that she did not witness Hunter doing drugs between Oct 6, when he purchased the gun, and Oct 22.
‘I’m afraid you are going to die’
The testimony could be helpful to Hunter’s defence, with Mr Lowell arguing prosecutors have not proved his client was using drugs during the period and did not consider himself an addict at the time.
However, earlier, Ms Biden told prosecutors she believed him to be high when she saw him that month.
In one text, days before the gun purchase, she told him: “I’m afraid you are going to die.”
Hunter, the first child of a sitting US president to be prosecuted, faces three federal charges of lying to a gun dealer, making a false claim on a gun background check and illegally possessing a gun.
He faces a second trial on tax charges in California in September.
The Biden family sought to show a united front during the trial in their home town, with friends and family filling several rows of the public gallery each day.
First Lady Jill Biden attended for several days before heading to France to join the president in commemorating the 80th anniversary of D-Day.
Hunter’s second wife, Melissa Cohen, has also been in court every day.
Earlier in the trial, which began on Tuesday, prosecutors elicited lurid testimony from two of Hunter’s other former romantic partners which is likely to feature in the 2024 presidential campaign.
Kathleen Buhle, Hunter’s ex-wife, told the court she discovered his drug use when she found a crack cocaine pipe in an ashtray on a porch at their home in Washington in 2015.
She described routinely searching his car for drugs before any of their three daughters drove the vehicle, “so they wouldn’t drive with drugs in it”.
Zoe Kestan, a former stripper, described hotel visits with Hunter Biden after meeting him at a gentlemen’s club in New York. She told the court he would want to smoke crack “as soon as he woke up” and would use the drug “every 20 minutes”.